Abstract
Leguminous plants (or Legumes, family Fabaceae) are known to form symbioses with extremely broad range of beneficial soil microorganisms (BSM), representing examples of almost all plant-microbe mutualistic systems. One of the most ecologically important and well-studied legume beneficial symbioses is root nodule (RN) symbiosis (symbiotic association with nitrogen-fixing bacteria). Compared with other interactions of legumes with BSM, RN symbioses demonstrate high level of genetic and metabolic integrity, which implies, inter alia, highly specific mutual recognition of partners. In this chapter, we describe the mechanisms of plant-microbe recognition during initial steps of RN symbiosis using the interaction of model legumes - pea (Pisum sativum L.), barrel medic (Medicago truncatula Gaertn.) and Lotus japonicus (Regel.) K. Larsen - with rhizobia as an example. We paid particular attention to symbiotic system of P. sativum since pea, besides its importance as a model object of genetics, is also a valuable crop plant. Hence, in conclusion, we discuss the potential to use obtained knowledge for optimizing the broad spectrum of plant adaptive functions and to improve the sustainability of legume crop production.
Keywords
- legume-rhizobial symbiosis
- Nod factor
- plant signaling
- genetic control
1. Introduction
Plants are attached immobile organisms and thus have to adapt to their environment in order to survive and reproduce successfully. Usually, plants experience multiple simultaneous impacts from different sources, so they developed complex signaling pathways to effectively detect these impacts and adequately respond to them [1]. Various microorganisms, which are constantly present in the environment, form one of the major factors affecting the life cycle of plants [2, 3]. Although many plant-associated microbes are pathogens that impair plant growth and reproduction, there are also a lot of beneficial (mutualistic) microorganisms able to provide plants with nutrition and additional defense mechanisms. Cooperation with such microorganisms constitutes the universal and highly effective strategy of plants’ ecological adaptation, so they tend to form long-lasting associations, which sometimes grow into highly integrated symbioses where one or both partners can develop novel features useful for their survival. Establishing of such symbiotic relationships involves the complicated developmental programs implemented under the joint control by plant and microbial partners and based on the cross-regulation of their genes.
Leguminous plants (or Legumes, family Fabaceae) are known to form symbioses with extremely broad range of beneficial soil microorganisms (BSM), representing examples of almost all plant-microbe mutualistic systems. One of the most ecologically important and well-studied legume-beneficial symbioses is root nodule (RN) symbiosis (symbiotic association with nitrogen-fixing bacteria). Compared with other interactions of legumes with BSM, RN symbioses demonstrate high level of genetic and metabolic integrity, which implies,
2. Legume-rhizobial symbiosis: An example of highly integrated plant-microbe system
Nitrogen is an essential component of all living systems, since it is part of the most important biological molecules – DNA and proteins. Molecular nitrogen (N2) in the atmosphere, despite being abundant, is extremely chemically inert and thus cannot be used by the majority of organisms, causing them to compete for more accessible nitrogen sources. Leguminous plants are able to grow in the soil/substrate without any combined nitrogen due to the fixation of atmospheric nitrogen by their symbiotic nodule bacteria (collectively called rhizobia) [4]. Nitrogen fixation occurs within special plant organs – root nodules (or, in some associations, also stem nodules). Development of these organs represents a well-organized process based on the tightly coordinated expression of specialized symbiotic plant and bacterial genes. The legume nodules provide an ecological niche for bacteria, as well as structure for metabolic/signal exchange between the partners and for the control of symbionts by the hosts [5].
Family Fabaceae contains about 19,000 species divided between three subfamilies (Caesalpinioideae, Mimosoideae, and Papilionoideae), with more than 700 genera of worldwide distribution [6]. With a single exception (
By contrast to legumes, their nitrogen-fixing microsymbionts do not constitute a taxonomically coherent group of organisms. The majority of rhizobia belong to the α-proteobacteria previously assigned to the
The development of nitrogen-fixing nodule is complex process that is traditionally divided into three major stages: preinfection, root colonization/nodule morphogenesis, and nitrogen fixation. On the first stage, the mutual recognition of partners occurs. The interaction between micro- and macrosymbiont begins with the activation of bacterial
The key stage of nodule development is conversion of bacteria into the form of intracellular symbionts through endocytosis-like process. Herein, the distal area of IT transforms into structure called infection droplet (ID), which releases membrane vesicles containing bacteria into plant cytoplasm. After leaving IT, rhizobia for some time retain their size and shape, subsequently differentiating into a specific form called bacteroids [18]. Compared to free-living bacteria, bacteroids have significantly (about 3-7 times) increased size and more complex shape, which can be round, pear-shaped, Y- or X-like, depending on specific symbiotic system. After the aforesaid differentiation, the synthesis of nitrogenase (the enzyme catalyzing reduction of N2 into NH4+) and other proteins involved in nitrogen fixation is activated in bacterial cells [19].
Bacteroids are embedded into a membrane structure named symbiosome, which are derived from membrane vesicle originating from ID. They are organelle-like units of plant cell responsible for nitrogen fixation. Symbiosome formation as well as bacteroid differentiation is induced by plant. Peri-bacteroid membrane (PBM) that surrounds bacteroids is an active interface of RN symbiosis where exchange of metabolites between symbionts occurs [19, 20]. Plant cells containing symbiosomes also undergo the deep differentiation, increasing the amount of their membrane structures (endoplasmic reticulum and the Golgi complex), which participate in the development of PBM and biosynthetic processes. Many proteins associated with nitrogen fixation appear in these cells
The developmental program described above is typical only for evolutionary advanced legumes belonging to the inverted repeat–lacking clade (IRLC) of Papilionoideae, such as
Several Papilionoideae members, such as
Such a complicated system of biological nitrogen fixation will work properly only when suitable partners meet each other in soil. This rendezvous becomes possible owing to reciprocal molecular signal exchange, which is not exhaustively studied to date.
2.1. Specificity of legume-rhizobial symbiosis
Root-nodule symbiosis is well known as highly specific plant-microbe interaction. According to the early surveys of symbiotic specificity [25], legumes were suggested to comprise a range of taxonomically restricted cross-inoculation groups (CIG) within which the free cross-inoculation occurs, while the species from different groups do not cross-inoculate.
The best studied examples of this classification are represented by four CIG: “
The analysis of CIG structure for both strictly and broadly specific legumes has shown that plant specificity towards rhizobia has good correlation with plant taxonomy on the genus or tribe level. It was also revealed that specificity of nodule formation does not correlate with symbiotic efficiency, i.e., efficiency of nitrogen fixation: several bacterial strains form normal nodules with one plant species, and are inactive (not able to fix nitrogen, Fix-) with another [26]. This could be due to the fact that nodulation is an early stage of symbiosis similar (and supposedly related) to pathogenic interaction, and is based on strict cross-activation of plant and bacterial genes (“gene-for-gene” interaction), while nitrogen fixation occurs on the later stages for which “gene-for-gene” interaction is not typical.
Moreover, it is specificity that makes possible the natural selection of effective
It is also important to note that the range of potential symbiotic partners can vary for both bacteria and plants. Symbiotic pair
2.2. Initial steps of rhizobium-legume symbiosis
The specificity of legume-rhizobia interactions is expressed mostly during the preinfection stage when rhizobia recognize the roots of appropriate host plants and colonize their surfaces. When the root-excreted signals (in particular, flavonoids) are perceived by bacteria, they activate the bacterial nodulation genes (
Rhizobia possess a wide range of genes involved in the early stages of nodulation, i.e., the NFs production [36]. Genes which are common to all rhizobia –
By perceiving the NF, plant starts various processes in root tissues. In particular, signaling molecule is required for the activation of plant genes in the epidermis cells and pericycle, as well as for mitotic reactivation of cortical cells and the formation of IT. Genes responsible for proper NF reception were first discovered in mutants of
Only in plants are LysM domains associated with a kinase-like domain [49] forming two main LysM-RLK gene families: the LYK family and the LYR family. All the LysM-RLKs are predicted to contain three LysM modules, although these modules exhibit a high degree of divergence, both within a protein and between proteins. It is considered that the initial function of LysM-RLKs has been recognition of chitin-based signal molecules produced by hostile microbes (termed as MAMPs (“microbe-associated molecular patterns”) or PAMPs (“pathogen-associated molecular patterns”)), similar to the function of CERK1 receptor-like kinase from
In
It is significant to note that NFR5 (and its homologs, NFP in
3. Molecular genetics of Nod-factor signaling in legumes
As reviewed in our recent publication [57], plant genes involved in development of RN symbiosis may be divided into two groups, according to approach which was used for the gene identification. The first group,
The large sizes of genomes of crop legumes (e.g., soybean or pea) in which the formal genetics of symbioses was initially developed, as well as low capability for genetic transformation, complicate greatly the cloning of symbiotic genes, analysis of their primary structures, and gene manipulations. Therefore, in the early 1990s,
The analysis of signaling pathway in RN symbiosis was started with experimental mutagenesis. Large-scale programs of insertion, chemical and X-rays mutagenesis, performed by different research groups, resulted in generation of numerous symbiotic mutants in
3.1. Nod-factor signaling in model legumes
After the first step of NF reception implemented by LysM-receptor kinases (described above), the symbiotic signal is transmitted to the pathway named Common Symbiosis Pathway (CSP), for it shares components with another interaction – arbuscular mycorrhiza (AM) symbiosis, the association with obligate biotrophic fungi of phylum
The first player in the CSP was identified more than 10 years ago. It is LRR-receptor kinase, or SymRK (symbiotic receptor kinase) described for
The symbiosis receptor kinase SymRK acts upstream of the NF-induced Ca2+ spiking in the perinuclear region of root hairs within a few minutes after NF application [79]. Perinuclear calcium spiking involves the release of calcium from a storage compartment (probably the nuclear envelope) through as-yet-unidentified calcium channels. To date, it is known that the potassium-permeable channels might compensate for the resulting charge imbalance and could regulate the calcium channels in plants [80-84]. Also, nucleoporins NUP85 and NUP133 (described only in
Ca2+ spikes are supposed to activate a calcium- and calmodulin-dependent protein kinase (CCaMK). This kinase contains an autoinhibition domain which, when removed, leads to a spontaneous activation of downstream transcription events and induction of nodule formation even in the absence of rhizobia [88]. Thus, CCaMK appears to be a general “manager” for both RN and AM symbioses and the last member of Common Symbiosis Pathway, because the next steps of nodulation signaling are independent from those of AM: the mutations in downstream
The CCaMK is known to form a complex with CYCLOPS, a phosphorylation substrate, within the nucleus [89].
It is supposed that CCaMK with help of CYCLOPS probably phosphorylates the specific transcription factors already present in cell, NSP1 and NSP2, which influence the changes of expression in several genes related to the symbiosis development [91, 92]. The activity of these proteins leads to the transcriptional changes in root tissues, for instance, increasing the level of early nodulins ENOD40, ENOD11, ENOD12, ENOD5, which are known to be the potential regulators of IT growth and nodule primordium formation [93-95]. Also, the changes in cytokinin status of plant are detected, followed by up-regulation of genes encoding for RN symbiosis-specific cytokinin receptors [96-98]. Moreover, transcription regulators NIN and ERN are to be induced specifically downstream of the early NF signaling pathway in order to coordinate and regulate the correct temporal and spatial formation of root nodules [99-102].
The presented genes are responsible for the signal cascade which is aimed to induce the nodulin genes involved in building the symbiotic structures and implementing their biochemical functions. It is supposed that this signaling pathway did not appear
Another important signaling process in RN symbiosis is an autoregulation of nodule formation. It takes place after successful mutual partners’ recognition and signal exchange. It is considered that legume host controls the root nodule numbers by sensing the external and internal cues. A major external cue is the concentration of soil nitrate, whereas a feedback regulatory system where nodules formed earlier suppress further nodulation through shoot-root communication is an important internal cue. The latter is known as the autoregulation of nodulation (AON), and is believed to consist of two long-distance signals: a root-derived signal that is generated in infected roots and transmitted to the shoot; and a shoot-derived signal that inhibits nodulation systemically [103-104]. Therefore, AON represents a strategy through which the host plant can balance the symbiotrophic N nutrition with the energetically more “cheap” combined N nutrition.
Recent findings on autoregulation of nodulation suggest that the root-derived ascending signals to the shoot are short peptides belonging to the CLE peptide family [105] [106]. The leucine-rich repeat receptor-like kinase HAR1 of
It was suggested that NF signaling induces expression or posttranslation processing of CLE peptides, which likely function as ascending long-distance signals to the shoot [110]. Thus, NF signaling is related to autoregulation as well, but in some indirect way. It is also worth noting that NF signaling pathway appears to work in mature nodules, since aforementioned “early nodulation genes” belonging to CSP, as well as NF receptor kinase genes, are highly expressed in nodule tissues (76, 111). Perhaps the active NF signaling is needed to prevent the induction of defense-like responses and/or to restrict the release of rhizobia into precise cell layers, thus regulating the formation of symbiotic interface [112].
3.2. Pea (Pisum sativum L.) as a unique example of increased specificity in plant-microbe interaction
Being one of the most ancient crops known to humanity, nowadays garden pea (
There are several pea genes known to participate in NFs’ reception, with the most interesting of them being
More than 20 years ago,
When
The comparison of
We proposed a model, based on the above, according to which the less specific “recognition” receptor (Sym10, perhaps in complex with other proteins) perceives the NF signal
4. Conclusion
Among all the multicellular eukaryotes, plants have the greatest need for the beneficial interaction with microorganisms, as they lack active movement and therefore cannot choose more advantageous habitat. That kind of restriction can be compensated by the ability of photosynthesis, as carbon compounds produced by plants are a significant stimulus for various microbes to cooperate with them. As a result of such cooperation, plant acquires an access to the adaptations of microsymbiont, and
The role of symbioses in the evolution of life, and plants in particular, cannot be underestimated. One can state that the tendency to establish mutually beneficial associations with microorganisms is an essential feature of plants, which has a wide variety of manifestations through a long coevolution of symbiotic partners. Photosynthesis itself, the main distinctive feature of plants, is provided by chloroplasts – the descendants of ancient symbiotic cyanobacteria. According to modern conception, plant colonization of land was possible primarily due to the symbiotic association with arbuscular mycorrhiza fungi. AM, in turn, is considered as a basis for the development of highly specific root-nodule symbiosis characteristic for legume plants. The possible path of the AM origin and its connection with RN was largely understood by studying
Emergence of Nod-factor signaling was among the most important factors that determined the evolutionary success of legume-rhizobial symbiosis. The wide variety of Nod-factors as well as finely tuned receptor system in plants ensure that only specific partners will meet each other in the soil and consequently form a superorganism with high level of genetic and metabolic integration. This appears to be a basis for evolution of the efficiency of symbiotic pairs, instead of single organisms – the results we now observe.
Legumes provide both an important food source for humanity and a unique model for investigation of the evolution and the underlying genetic mechanisms of mutualistic plant-microbe symbioses. Further studies of the genetic bases of signal interactions between plants and microbes can provide more information about evolution of such a mutually beneficial association, as well as about spreading of the legumes across the world. Discovery of genes involved in recognition of partners, transduction of symbiotic signals and overall “management” of symbiosis will also provide a useful tool for agriculture, as the knowledge obtained from this studying will facilitate the creation of highly-effective specific symbiotic pairs between crop plants and nitrogen-fixing bacteria in field..
Acknowledgments
A.S. Sulima was financially supported by the grant of Russian Foundation for Basic Research (RFBR) # 14-04-32289_mol-a. V.A. Zhukov, O.Y. Shtark, A.Y. Borisov, and I.A. Tikhonovich were financially supported by the grant of Russian Science Foundation (RSF) # 14-24-00135. The authors thank Dr. M.N. Povydysh (Saint-Petersburg State Chemical Pharmaceutical Academy, St.Petersburg, Russia) for help in preparation of figures.
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